The plant immune system: From discovery to deployment

Cell, Journal Year: 2024, Volume and Issue: 187(9), P. 2095 - 2116

Published: April 1, 2024

Plant diseases cause famines, drive human migration, and present challenges to agricultural sustainability as pathogen ranges shift under climate change. breeders discovered Mendelian genetic loci conferring disease resistance specific isolates over 100 years ago. Subsequent breeding for underpins modern agriculture and, along with the emergence focus on model plants genetics genomics research, has provided rich resources molecular biological exploration last 50 years. These studies led identification of extracellular intracellular receptors that convert recognition microbe-encoded patterns or pathogen-delivered virulence effectors into defense activation. receptor systems, downstream responses, define plant immune systems have evolved since migration land ∼500 million Our current understanding provides platform development rational enhancement control many continue plague crop production.

Language: Английский

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Viruses inhibit TIR gcADPR signalling to overcome bacterial defence

Nature, Journal Year: 2022, Volume and Issue: 611(7935), P. 326 - 331

Published: Sept. 29, 2022

Language: Английский

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Shared TIR enzymatic functions regulate cell death and immunity across the tree of life

Science, Journal Year: 2022, Volume and Issue: 377(6605)

Published: July 7, 2022

In the 20th century, researchers studying animal and plant signaling pathways discovered a protein domain that is shared across diverse innate immune systems: Toll/interleukin-1/resistance gene (TIR) domain. The TIR found in several architectures was defined as an adaptor mediates protein-protein interactions immunity developmental pathways. However, studies of nerve degeneration animals-and subsequent breakthroughs plant, bacterial, archaeal systems-revealed domains possess enzymatic activities. We provide synthesis functions role various related products evolutionarily systems. These may ultimately guide interventions would span tree life, from treating human neurodegenerative disorders bacterial infections to preventing diseases.

Language: Английский

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Cyclic ADP ribose isomers: Production, chemical structures, and immune signaling

Science, Journal Year: 2022, Volume and Issue: 377(6614)

Published: Sept. 1, 2022

Cyclic adenosine diphosphate (ADP)–ribose (cADPR) isomers are signaling molecules produced by bacterial and plant Toll/interleukin-1 receptor (TIR) domains via nicotinamide adenine dinucleotide (oxidized form) (NAD + ) hydrolysis. We show that v-cADPR (2′cADPR) v2-cADPR (3′cADPR) cyclized O-glycosidic bond formation between the ribose moieties in ADPR. Structures of 2′cADPR-producing TIR reveal conformational changes lead to an active assembly resembles those Toll-like adaptor domains. Mutagenesis reveals a conserved tryptophan is essential for cyclization. 3′cADPR activator ThsA effector proteins from antiphage defense system termed Thoeris suppressor immunity when HopAM1. Collectively, our results molecular basis cADPR isomer production establish bacteria as antiviral immunity–suppressing molecule.

Language: Английский

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Effector‐dependent activation and oligomerization of plant NRC class helper NLRs by sensor NLR immune receptors Rpi‐amr3 and Rpi‐amr1

The EMBO Journal, Journal Year: 2023, Volume and Issue: 42(5)

Published: Jan. 2, 2023

Abstract Plant pathogens compromise crop yields. Plants have evolved robust innate immunity that depends in part on intracellular Nucleotide‐binding, Leucine rich‐Repeat (NLR) immune receptors activate defense responses upon detection of pathogen‐derived effectors. Most “sensor” NLRs detect effectors require the activity “helper” NLRs, but how helper support sensor NLR function is poorly understood. Many Solanaceae NRC (NLR‐Required for Cell death) class NLRs. We show here Rpi‐amr3, a from Solanum americanum , detects AVRamr3 potato late blight pathogen, Phytophthora infestans and activates oligomerization NRC2 NRC4 into high‐molecular‐weight resistosomes. In contrast, recognition P. effector AVRamr1 by another Rpi‐amr1 induces formation only resistosome. The activated oligomer becomes enriched membrane fractions. ATP‐binding motifs both Rpi‐amr3 are required resistosome formation, not interaction with its cognate effector. can be homologs other species. Mechanistic understanding will underpin engineering crops durable disease resistance.

Language: Английский

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NLR receptors in plant immunity: making sense of the alphabet soup

EMBO Reports, Journal Year: 2023, Volume and Issue: 24(10)

Published: Aug. 21, 2023

Plants coordinately use cell-surface and intracellular immune receptors to perceive pathogens mount an response. Intracellular events of pathogen recognition are largely mediated by the nucleotide binding leucine rich-repeat (NLR) classes. Upon perception, NLRs trigger a potent broad-spectrum reaction, usually accompanied form programmed cell death termed hypersensitive Some plant act as multifunctional singleton which combine detection signaling. However, can also function in higher order pairs networks functionally specialized interconnected receptors. In this article, we cover basic aspects NLR biology with emphasis on networks. We highlight some recent advances structure, function, activation discuss emerging topics such modulator NLRs, suppression bioengineering. Multi-disciplinary approaches required disentangle how these receptor evolve. Answering questions holds potential deepen our understanding system unlock new era disease resistance breeding.

Language: Английский

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Oligomerization of a plant helper NLR requires cell-surface and intracellular immune receptor activation

Proceedings of the National Academy of Sciences, Journal Year: 2023, Volume and Issue: 120(11)

Published: March 6, 2023

Plant disease resistance involves both detection of microbial molecular patterns by cell-surface pattern recognition receptors and pathogen effectors intracellular NLR immune receptors. NLRs are classified as sensor NLRs, involved in effector detection, or helper required for signaling. TIR-domain-containing (TNLs) require NRG1 ADR1 resistance, activation defense requires the lipase-domain proteins EDS1, SAG101, PAD4. Previously, we found that associates with EDS1 SAG101 a TNL activation-dependent manner [X. Sun et al. , Nat. Commun. 12 3335 (2021)]. We report here how itself during TNL-initiated immunity. Full immunity coactivation mutual potentiation receptor-initiated signaling [B. P. M. Ngou, H.-K. Ahn, Ding, J. D. G. Jones, Nature 592 110–115 (2021), Yuan 105–109 find while TNLs is sufficient to promote NRG1–EDS1–SAG101 interaction, formation an oligomeric resistosome additional defense. These data suggest vivo part mechanism links receptor pathways.

Language: Английский

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Plant and prokaryotic TIR domains generate distinct cyclic ADPR NADase products

Science Advances, Journal Year: 2023, Volume and Issue: 9(11)

Published: March 17, 2023

Toll/interleukin-1 receptor (TIR) domain proteins function in cell death and immunity. In plants bacteria, TIR domains are often enzymes that produce isomers of cyclic adenosine 5′-diphosphate–ribose (cADPR) as putative immune signaling molecules. The identity functional conservation cADPR isomer signals is unclear. A previous report found a plant could cross-activate the prokaryotic Thoeris TIR–immune system, suggesting TIR-immune signals. Here, we generate autoactive TIRs test converse hypothesis: Do also immunity? Using planta vitro assays, find overlapping sets further clarify how activate system via producing 3′cADPR. This study demonstrates requirements for systems distinct across kingdoms diversity small-molecule products.

Language: Английский

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NLR signaling in plants: from resistosomes to second messengers

Trends in Biochemical Sciences, Journal Year: 2023, Volume and Issue: 48(9), P. 776 - 787

Published: June 30, 2023

Pathogen effector-induced assembly of resistosomes has been established as an important event for nucleotide binding and leucine-rich repeat-containing receptor (NLR) signaling in plants.The pentameric coiled-coil domain-containing NLR (CNL) act Ca2+-permeable channels, whereas the tetrameric Toll-interleukin 1-like (TIR) (TNL) are NADase holoenzymes.TNL catalyze production nucleotide-derived second messengers to activate downstream helper NLRs activated disease resistance 1 (ADR1) N requirement gene (NRG1) CNL class. Thus, CNLs TNLs converge on Ca2+ signals trigger plant immunity.NLR cross-talks with pattern-triggered immunity (PTI) pathways.NLR pathways plants negatively regulated by both hosts pathogens. Nucleotide receptors (NLRs) have a critical role through direct or indirect recognition pathogen effectors. Recent studies demonstrated that such induces formation large protein complexes called mediate immune signaling. Some influx acting others function active NADases messengers. In this review we summarize these resistosome-mediated derivatives. We also discuss events regulation resistosome Plants rely multiple detect invading microbial pathogens mount responses [1.Ngou B.P.M. et al.Thirty years resistance: zig-zag system.Plant Cell. 2022; 34: 1447-1478Crossref PubMed Scopus (45) Google Scholar,2.Zhou J.M. Zhang Y. Plant immunity: danger perception signaling.Cell. 2020; 181: 978-989Abstract Full Text PDF (328) Scholar]. One subfamily pattern-recognition (PRRs) (see Glossary) at cell surface Scholar, 2.Zhou 3.DeFalco T.A. Zipfel C. Molecular mechanisms early signaling.Mol. 2021; 81: 3449-3467Abstract (0) PRRs recognize pathogen-associated molecular patterns (PAMPs) host-derived damage-associated (DAMPs), leading (PTI). PTI constitutes first line inducible defense against can breach layer secreting effector proteins into cells dampen PTI. To counteract virulence activity effectors, evolved receptors: intracellular NLRs. specifically proteins, inducing effector-triggered (ETI) confer race-specific site entry Scholar,4.Jones J.D.G. al.Intracellular innate surveillance devices animals.Science. 2016; 354aaf6395Crossref different structures subcellular localizations but conserved responses, including influx, bursts reactive oxygen species (ROS), phytocytokines phytohormones, transcriptional reprogramming Probably reason, ETI tightly connected [5.Yuan M. al.Pattern-recognition required NLR-mediated immunity.Nature. 592: 105-109Crossref (351) Scholar,6.Ngou al.Mutual potentiation cell-surface receptors.Nature. 110-115Crossref (329) However, differ timing, amplitude, duration defense, which could be determining their physiological outcomes. addition includes hypersensitive response (HR), form rapid localized programmed death infection [7.Jones J.D. Dangl J.L. The system.Nature. 2006; 444: 323-329Crossref (8693) largest hundreds distinct members [4.Jones two domains: central nucleotide-binding oligomerization domain (NOD), C-terminal repeat (LRR) domain. A variable (CC) is attached terminus, resulting TIR-NLR CC-NLR (CNL), respectively [8.Maruta N. al.Structural basis activation signalling plants.Immunogenetics. 74: 5-26Crossref (25) Scholar,9.Hu Z. Chai J. Assembly architecture inflammasomes.Annu. Rev. Biophys. 52: 8.1-8.22Google pathogen-sensing NLRs, there some (h) translate from [10.Feehan al.Plant get little help friends.Curr. Opin. Biol. 56: 99-108Crossref (18) Scholar,11.Jubic L.M. al.Help wanted: responses.Curr. 2019; 50: 82-94Crossref (139) Examples hNLRs include Resistance Powdery Mildew 8 (RPW8) family [12.Wu al.Differential TNL-mediated redundant CNLs.New Phytol. 222: 938-953Crossref (118) 13.Castel B. al.Diverse defence via RPW8-NLR NRG1.New 966-980Crossref (144) 14.Qi T. al.NRG1 functions EDS1 regulate TIR-NLR-mediated Nicotiana benthamiana.Proc. Natl. Acad. Sci. U. S. A. 2018; 115: E10979-E10987Crossref (121) 15.Collier S.M. al.Cell mediated N-terminal domains unique highly class NB-LRR protein.Mol. Microbe Interact. 2011; 24: 918-931Crossref (230) Scholar] (Figure 1) (NRCs) [16.Adachi H. Kamoun networks plants.Essays Biochem. 66: 541-549Crossref (4) Scholar,17.Wu C.H. al.NLR network mediates diverse pathogens.Proc. 2017; 114: 8113-8118Crossref (211) More recent signaling, many sensor Solanaceae, depends NRCs upon [18.Ahn H.K. al.Effector-dependent NRC Rpi-amr3 Rpi-amr1.EMBO 2023; 42e111484Crossref (5) Scholar,19.Contreras M.P. al.Sensor helpers pathogens.EMBO 42e111519PubMed messengers, calcium ion derivations. crosstalk between negative effectors host regulators. directly indirectly. For example, interaction benthamiana TNL Roq1 (recognition XopQ its recognized (Xanthomonas outer Q) [20.Schultink al.Roq1 Xanthomonas Pseudomonas HopQ1.Plant 92: 787-795Crossref (82) Scholar,21.Martin R. al.Structure ROQ1 recognizing XopQ.Science. 370eabd9993Crossref (174) Scholar], arabidopsis RPP1 Peronospora parasitica ATR1 (Arabidopsis thaliana [22.Ma al.Direct pathogen-induced complex holoenzyme.Science. 370abe3069Crossref (169) Scholar,23.Krasileva K.V. al.Activation Arabidopsis specified planta association cognate oomycete effector.Plant 2010; 22: 2444-2458Crossref (220) wheat Sr35 (stem rust 35) AvrSr35 [24.Zhao Y.-B. al.Pathogen triggers mechanism.Sci. Adv. 8eabq5108Crossref (13) 25.Forderer al.A defines common principles channels.Nature. 610: 532-539Crossref 26.Salcedo al.Variation determines stem race Ug99.Science. 358: 1604-1606Crossref (117) spp, Hyaloperonospora parasitica, Puccinia graminis tritici, respectively. monitoring effector-mediated perturbations targets. example ZAR1 (HOPZ-ACTIVATED RESISTANCE [27.Lewis al.Allele-specific attenuation syringae HopZ1a type III protein.PLoS Genet. 6e1000894Crossref (111) exists preformed kinase RKS1 (resistance-related normal conditions recognizes AvrAC indirectly uridylylation another PBL2 (PBS1-like 2) [28.Wang al.Ligand-triggered allosteric ADP release primes complex.Science. 364aav5868Crossref (231) Scholar,29.Wang G. al.The decoy substrate pseudokinase specify modified-self plants.Cell Host Microbe. 2015; 18: 285-295Abstract (156) Scholar]; AvrAC-uridylylated associates consequently activates ZAR1-mediated immunity. Alternatively, cases, may not necessarily CHS3 (CHILLING SENSITIVE 3)/CSA1 (CONSTITUTIVE SHADE-AVOIDANCE pair detects PRR coreceptor BAK1 (BRASSINOSTEROID INSENSITIVE 1-associated [30.Yang al.Allelic variation CHS3/CSA1 reveals functional cell-death regulatory modes.Cell 30: 1701-1716Abstract (7) malectin-like receptor-like LET1 autoimmunity SUMM2 (SUPPRESSOR OF MKK1 MKK2) MEKK2 (MAP/ERK kinase-2) scaffolding [31.Liu LETUM1 modulates scaffolding.Nat. Plants. 6: 1106-1115Crossref (26) Effector leads termed 1). Cryoelectron microscopy (cryoEM) analyses show containing ZAR1, RKS1, uridylylated (PBL2UMP) forms wheel-like [32.Wang al.Reconstitution structure conferring immunity.Science. 364aav5870Crossref (368) 1, left). Pentamerization mainly NOD module PBL2UMP being presented rim wheel 2). contrast AvrSr35, remarkably similar Scholar,25.Forderer more study showed oligomeric NRG1 likely formed plasma membrane (PM) [33.Feehan al.Oligomerization requires activation.Proc. 120e2210406120Crossref (3) Interestingly, resistosomes, underlying await further elucidation By comparison, end results right). induced [21.Martin As seen primarily Structural modeling sequestered inactive Scholar,24.Zhao Scholar,32.Wang suggesting oligomerization. it remains unknown whether all resistosomes. Many pairs, executor initiating [34.Xi al.Insight mode action paired receptors.Essays 513-526Crossref (2) Whether how represent challenge understanding mechanisms. cryoEM resistosome, five α1-helices solvent-exposed shaped like channel pore Functional data support ETI. Importantly, electrophysiological evidence supports [35.Bi calcium-permeable triggering 184: 3528-3541Abstract (181) bottom Single molecule imaging hours before loss PM integrity These suggest acts α1 distantly related [36.Adachi al.An motif functionally across species.eLife. 8e49956Crossref (92) Ca2+-channel among Indeed, bears [25.Forderer essential helix well-defined resistosome. It environment funnel-shaped localization shown RPM1 (resistance pv. maculicola [37.El Kasmi F. al.Signaling plasma-membrane self-association full-length protein.Proc. E7385-E7394Crossref (70) RPS2 P. [38.Axtell M.J. Staskawicz B.J. Initiation RPS2-specified coupled AvrRpt2-directed elimination RIN4.Cell. 2003; 112: 369-377Abstract (643) bethamiana Tm-22 [39.Wang NB-ARC domain-mediated CC domain.PLoS Pathog. 16e1008475Crossref (20) ZAR1-like examined. TNL-activated hNLRs, NRG1s, ADR1s display autoactive Scholar,40.Jacob "helper" nonselective cation channels.Science. 373: 420-425Crossref (125) indicating Solanaceae (SD) found noncanonical [41.Seong K. al.Evolution genes wild tomato species.New 227: 1530-1543Crossref (36) themselves structures. undetermined activity. Multiple lines extracellular [42.Xu tale families: channels immunity.Plant 1551-1567Crossref (19) Scholar,43.Kim N.H. al.Con-Ca2+-tenating channels.New 234: 813-818Crossref (8) Elevation concentrations one earliest during Gain-of-function mutations CNGC19/20 (CYCLIC NUCLEOTIDE GATED CHANNEL19/20) increased constitutively (enhanced susceptibility 1)- SA (salicylic acid)-dependent [44.Yu X. kinases BAK1/SERK4 channel-mediated cellular homeostasis containment.Curr. 29: 3778-3790Abstract (64) Scholar,45.Zhao mis-regulated cyclic nucleotide-gated cytosolic elevation Arabidopsis.New 230: 1078-1094Crossref (33) Unregulated Sr35, NRG1, ADR1 sufficient recapitulate CNL-mediated eukaryotic Although released internal pools contribute pharmacological blocking compartments ruthenium red (RR) less efficient inhibition HR than blocker LaCl3 [46.Gao heat-activated 6 involved heat shock responses.Plant 2012; 70: 1056-1069Crossref supporting notion major responses. Nuclear [47.Ludke D. yet? Nucleocytoplasmic coordination immunity.New 236: 24-42Crossref mechanism associated enigmatic. Several interact factors [48.Wang al.Diversity, receptors.J. Integr. 63: 283-296Crossref (11) programming nucleus. transcription set genes, other reprogramming. NRG1A PM- nucleus-localized activation, only PM-resident oligomers oligomerization-independent function. Increases nuclear free reported various stresses [49.Pauly nucleus together cytosol generates specific signatures tobacco suspension culture cells.Cell Calcium. 2001; 413-421Crossref 50.van Der Luit A.H. al.Distinct calmodulin expression tobacco.Plant Physiol. 1999; 121: 705-714Crossref 51.Xiong T.C. al.Isolated nuclei mechanical thermal sensors signalling.Plant 2004; 40: 12-21Crossref should kept mind spatial distribution uniform, steep gradients few nanometers away [52.Pangršič al.EF-hand buffers exocytosis sensory hair cells.Proc. E1028-E1037Crossref transported PM-localized and/or reach possible continuum organelle endoplasmic reticulum (ER). Such result An CNGC15 symbiotic oscillation [53.Charpentier al.Nuclear-localized oscillations.Science. 352: 1102-1105Crossref While signals, they TNLs, CNLs, NADases. ATR1-induced significantly enhances activity, holoenzyme enzymatic encoded TIR [54.Wan L. al.TIR NAD+-cleaving enzymes promote death.Science. 365: 799-803Crossref (226) Scholar,55.Horsefield al.NAD+ cleavage animal pathways.Science. 793-799Crossref (244) TIR-only bacterial HopBA1 (RBA1) [56.Nishimura M.T. al.TIR-only RBA1 Arabidopsis.Proc. E2053-E2062Crossref (93) Tetramerization composite sites Scholar,22.Ma [57.Shi SARM1 recognition, small molecules.Mol. 82: 1643-1659Abstract (27) 58.Manik M.K. al.Cyclic ribose isomers: production, chemical structures, signaling.Science. 377eadc8969Crossref 59.Hogrel nucleotide-induced helical effector.Nature. 608: 808-812Crossref analogs PAD4 (phytoalexin deficient 4)

Language: Английский

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Pathogen perception and signaling in plant immunity

The Plant Cell, Journal Year: 2024, Volume and Issue: 36(5), P. 1465 - 1481

Published: Jan. 23, 2024

Abstract Plant diseases are a constant and serious threat to agriculture ecological biodiversity. Plants possess sophisticated innate immunity system capable of detecting responding pathogen infection prevent disease. Our understanding this has grown enormously over the past century. Early genetic descriptions plant disease resistance virulence were embodied in gene-for-gene hypothesis, while physiological studies identified pathogen-derived elicitors that could trigger defense responses cells tissues. Molecular these phenomena have now coalesced into an integrated model involving cell surface intracellular detection specific molecules proteins culminating induction various cellular responses. Extracellular receptors engage distinct signaling processes but converge on many similar outputs with substantial evidence for integration pathways interdependent networks controlling outcomes. Many molecular details recognition known, providing opportunities bioengineering enhance protection from Here we provide overview current main principles immunity, emphasis key scientific milestones leading insights.

Language: Английский

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